DOMINANCE RELATIONSHIPS IN CAPTIVE MALE BARE-TAILED WOOLLY OPOSSUM (CALUROMYS PHIIANDER, MARSUPIALIA: DIDELPHIDAE)

M.-L. GUILLEMIN*, M. ATRAMENTOWICZ* & P. CHARLES-DOMINIQUE*

RÉSUMÉ

Au cours de ce travail nous avons voulu tester en captivité l'importance du poids corporel dans l'établissement de relations de dominance chez les mâles Caluromysphilander, chez qui des compétitions inter-mâles ont été étudiées. Les comportements et l'évolution de différents paramètres physiologiques ont été observés durant 18 expérimentations effectuées respectivement sur 6 groupes de deux mâles et sur 12 groupes de deux mâles et une femelle. Des relations de dominance-subordination se mettent en place même en l'absence de femelle, mais la compétition est plus forte dans les groupes comprenant une femelle. Dans ces conditions expérimentales, le rang social est basé principalement sur le poids et l'âge. Lorsque la relation de dominance est mise en place, le rang social des mâles est bien défini et il reste stable jusqu'à la fin de l'expérimentation. Ces relations de dominance stables pourraient profiter aux dominants et aux dominés en minimisant les risques de blessures sérieuses. Les mâles montrent des signes typiques caractérisant un stress social : une baisse du poids et de l'hématocrite, les dominés étant plus stressés que les dominants. Chez les mâles dominants, la baisse de l'hématocrite est plus faible que chez les dominés, et la concentration de testostérone dans le sang diminue plus que chez les dominés. Au niveau comportemental, les dominants effectuent la plupart des interactions agonistiques << offensives » et plus d'investigations olfactives de leur environnement (flairage-léchage) que les dominés. De plus, leurs interactions avec les femelles sont plus nombreuses et moins agressives que celles des dominés.

SUMMARY

In this study, we test the hypothesis thal body size is a key factor in determining dominance relationships during agonistic encounters between captive males Caluromys philander, and male-male competition was experimentally tested. Physiological and behav­ ioural parameters were investigated during 18 experimental trials including two males alone (6), and two males with a female (12). A dominance-submission relationship exists even with no female, although competition is stronger when a female is present. Dominance is based on age and body mass in C. philander under experimental conditions. When dominance was settled, dominance rank was clear eut and consistent during ali the experimentation. Stable dominance-subordination relationships may benefit both dominants and subordinates by minimizing the incidence of serious wounds. Males show typical signs of social stress: bath body weight and hematocrit rate decrease, but subordinates are more stressed than dominants.

* CNRS, UMR 8571, Muséum National d'Histoire Naturelle, Laboratoire d'Écologie Générale, 4, avenue du Petit Château, 91800 Brunoy, France.

Rev. Écol. (Terre Vie), vol. 55, 2000.

337 Dominant males exhibit a lower decrease in hematocrit rate and a higher decrease in testosterone concentration in blood. They display most of the "aggressive" behaviours, scan more actively the experimental cages and engage in fewer aggressive interactions with females in comparison with subordinate males.

INTRODUCTION

Competition among males for access to females is often characterized by combats and aggressive interactions. These aggressive interactions are expected to play a major role in determining reproductive success of males (Krebs & Davies, 1997). But, under certain ecological conditions, mate searching by males could supersede combat as the primary mode of competition. This "scramble competi­ tion" polygyny has been first demonstrated in insects (Alcock, 1980) and seems important in sorne species of asocial mammals (Schwagmeyer, 1988). Even if combat and mate searching seem to be two contradictory modes of competition, in sorne species these two competition modes could coexist. For example, in sorne species searching is a prerequisite for acquiring mating opportunities. However, if numerous males accumulate around the same female before the onset of the œstrus, aggressive interactions can determine final suécess in mating (review in Schwagmeyer, 1988). Didelphids in general retain numerous ancestral morphological and physi­ ological traits (Charles-Dominique, 1983; Atramentowicz, 1986; Holmes, 1987). For these reasons, many authors have proposed that their social behaviour is more or Jess identical to that of their ancestors (Holmes,l 987). Social interactions have been well investigated in only one didelphid species: Didelphis virginiana (Holmes, 1987; Ryser, 1990). In this species Holmes (1987) and Ryser (1990) determined that captive and wild animais perform a stable social hierarchy, with male social status associated with body mass and testosterone concentration in plasma. Various features are associated with dominance in D. virginiana, including access to resources (food and mate) and scent marking (Holmes, 1987). In nature, females D. virginiana are followed by numerous males (up to five males; Ryser, 1990) from several days to several hours before the œstrus. This precopulatory accumulation of males around a female have also been recorded in the wild for another didelphid species: Philander opossum (Charles-Dominique, pers. obs.). The Bare-tailed Woolly Opossum (Caluromys philander) is a polygynous species. This noctumal, arboreal and solitary species is widely distributed in the northem and eastern regions of South America (Atramentowicz, 1988). Animais do not defend a territory, and male and female home range largely overlaps (Charles-Dominique, 1983; Julien-Laferrière, 1995). Individuals communicate through olfactory and auditory pathways, as in most noctumal species (Russell, 1984). In the Bare-tailed Wo olly Opossum social bonds are limited and hierarchy is not obvious. As in the other didelphid species, interactions between conspecifics are few, often aggressive, except during mating or mother/offspring relationships. Nevertheless, Caluromys occupies a special place among didelphid species, with a higher encephalisation quotient, related to arboreality (Eisenberg & Wilson, 1981), and extended mother-offspring relationships (Atramentowicz, 1986). Evi­ dence of inter-male competition to gain access to œstrous females has not been experimentally demonstrated, although it has been observed in the field (Charles­ Dominique, 1983).

338 In this study, we test the hypothesis that body size is a key factor in deterrnining dominance relationships during agonistic encounters between captive males C. philander. Experimental trials were performed in testing cages using paired males including, or not, a female. Morphological and hormonal correlates of dominance were assessed and we postulated that subordinate males would exhibit lower levels of testosterone and poorer physical conditions at the end of the encounter compared to dominant males.

MATERIAL AND METHODS

ANIMALS

In this study, 12 females and 15 males Caluromys philander were used. AU of them were sexually mature (more than seven months) and born in captivity at the laboratory of Écologie Générale, M.N.H.N. (Brunoy, France). Owing to the little number of animais in our breeding colon y, males were used in more than one experiment. These males, used in more than one experiment, were individually housed for at least four weeks between two experimental trials. The diet consisted in fruit (apples, bananas and oranges) and a mixture of milk, baby cereal and protein-rich powder. Water was available ad libitum. Temperature (25 °C), hygrometry (50 %) and light period (12 h) remained constant throughout the year. In order to facilitate observations, animais were maintained in a reverse daylight.

EXPERIMENTAL DESIGN

Animais were housed in three adjacent cages (149 x 64 x 58 cm), each provided with a wooden nest-box and branches to allow locomotion activity for this arboreal species. Cages could be connected together, by opening doors. Doors were opened 48h each week during a four-week period. Therefore, the animais of an experimental trial could meet each other only during two consecutive days by week. Three experimental trials were monitored simultaneously in three separate rooms. Males were paired according to body mass differences. Both males were either about the same body mass (on average a 25 g difference, maximum = 50 g difference) or of different body mass (on average a 100 g difference, minimum = 80 g difference). In this species where adult body mass in males ranges from 300 to 500 g, these differences represented from 8 to 20 % of total body mass. Reference experiments were monitored with two males alone, and later on, another with two males and a female. Eighteen groups were tested: six groups with males alone, including four groups of different body mass and two groups of similar body mass; and 12 groups with two males and a female, including eight groups with males of different body mass and four groups with males of similar body mass.

PHYSIOLOGICAL MEASUREMENTS

Body mass was recorded weekly, two days before the beginning of the experiments. Blood sample of males was taken by puncture of the saphenous vein.

- 339 - After centrifugation, hematocrit was measured and testosterone plasma concen­ tration was determined by radioimmunoassay. We used samples of 50 �-tl plasma and the procedure described by Perret & Atramentowicz (1989). The mean intra-assay coefficient of variation based on ali samples tested in duplicate was 6.3 % (± 4.2) and the mean inter assay coefficient was 8.5 % (± 5.9) based on 25 samples with testosterone concentrations averaging 5 ng/ml. Uro-genital smears were coliected in females twice a week, to detect œstrous occurrence.

BEHAVIOURAL OBSERVATIONS

Animais were observed in their cage for one hour foliowing daylight switch off, with a dim red light suitable for noctumal species. To aliow sequential observations in three rooms, daylight was switched off delayed successively in each room. Observations were conducted for two consecutive days each week, when experimental cages were connected together. Ali individual behaviours were recorded: eating, drinking, excreting, groom­ ing, scent-marking (urine deposit or rubbing the penis along branches) and smeliing-licking (the animal smelis the air or a branch with slight head movements or lick the branches). Interactions between individuals, described in table 1, were noted as foliow: - neutra! or affiliative (indifference, approach, close proximity, licking or smeliing)

TABLE 1 Social behaviour patterns in the Bare-tailed Wo olly Op ossum (Caluromys philander).

Behaviour Description

Neutra! or affi liative Indifference An animal stays motionless or carries on his behaviour when a conspecific makes any type of active social behaviour such as an approach or a threat Approach Walking towards another animal Close proximity Staying close to a conspecific (Jess than 0.1 rn) Licking or smelling Olfactory investigation of the body or of the ana-genital area of a conspecific Antagonistic offensive Threat Emission of a "hiss" often associated with the typical opened mouth posture Aggression An animal jumps on its opponent and tries to bit him Chasing An animal runs after its opponent defensive Escape Running away from the opponent Avoidance Walking away from another animal Distress calls Loud distress cali varying from a weak "hiss" to a loud "ki-hein", emitted in situation of pain or intense aggression Sexual Sexual chasing The male follows, or runs after, the female Mating attempt The male tries to immobilize the female using his fore legs and mouth

340 - antagonistic (threat, aggression, chasing, escape, avoidance, distress calls) - sexual (sexual chasing, mating attempt)

A dominance index Id and an activity rate A were calculated for each male. Id= number of offensive behaviours (chasing, threatening, physical aggression)/total number of agonistic behavioural acts (offensive + defensive). A = total number of behavioural acts per hour (individual behaviours and interactions). The dominance index, calculated for each individual of a dyad, corresponds to the hierarchical index established by Coulon (1975, in Yahyaoui et al., 1995). This index varies from 0 in animais which exhibit only defensive behaviours to 1 in animais which exhibit only offensive behaviours. The differences between the Id of the two males are calculated for each experiment. In dyads where this difference was 0.5 or more we considered that a dominance-subordination relationship was settled. In these groups, the male with the greatest Id was considered as the dominant and the other male as the subordinate.

STATISTICAL PROCEDURES

All values are means ± standard deviations. To compare different groups we used Kruskall-Wallis tests and multiple comparisons. Comparisons between two groups were made with Mann-Whitney and Wilcoxon tests. Spearman tests were used to evaluate correlations between specifie parameters.

RESULTS

DOMINANCE-SUBORDINATION RELATIONSHIPS BETWEEN MALES

Female presence was not necessary to enhance a dominance relationship since it was observed in reference groups (two males alone, Table II). In only two groups Id was below 0.5, meaning a lack of established dominance-submission relationship between males (Table Il). These four males appeared significantlyless active compared to other males (A = 32 ± 17 and A = 79 ± 34 respectively; U test, p < 0.01; Table Il). Male-male interaction rate was 15 ± 11 interactions per hour and mainly included agonistic interactions (84 %). In nine groups, since the beginning of the experiment, one male exhibited essentially offensive behaviours whereas the other behaved as a subordinate and dominance took place without any fight. In seven groups a dominance relationship took place after 1 to 62 fights (total observed per groups). In these groups, bath males exhibited, firstly, as many offensive behaviours (threat, chasing, attack) as defensive ones (escape, run away, distress calls). Fights usually occurred on the ground or bath males hanging under a branch using their prehensile tail. Serious wounds may result, especially biting. Then fights briefly ceased and afterwards only the dominant male displayed offensive agonistic behaviours, the other male exhibiting defensive behaviours. Thus we considered that the dominance­ submission relation was established. In any case, once the relationship was

- 341 TABLE Il

Dominance index (Id) and activity rate (A) calculated fo r each male in experimental . groups. The total number of agonistic behavioural acts are noted into parenthesis. In two groups, noted in shaded areas, the dominance-submission relationship was not established (Id 1 -Id 2 < 0.5).

A) Reference group: two males alone male 1 male 2 Id 1 A Id 2 A Id 1-Id2

males of 0.80 (44) 63 0.30 (62) 18 0.50 different body 1.00 (3 1) 62 0.00 (89) 66 1.00 mass N = 4 1.00 (58) 50 0.00 (154) 88 1.00 0.60 (28) 45 0.37 (8) 8 0.23

males of similar 0.96 (81) 138 0.02 (220) 103 0.94 body mass N = 2 1.00 (103) 185 0.06 (274) 63 0.94

B) Two males and a female male 1 male 2 Id 1 A Id 2 A Id l-Id2

1.00 (3) 86 0.00 (6) 86 1.00 0.80 (34) 71 0.00 (99) 103 0.80 males of 0.84 (19) 7 0.00 (23) 47 0.84 different body 0.65 (17) 67 0.00 (69) 58 0.65 mass N = 8 0.86 (61) 102 0.05 (136) 56 0.81 0.97 (138) 119 0.01 (193) 83 0.96 1.00 (83) 135 0.45 (138) 69 0.55 1.00 (33) 60 0.00 (90) 73 1.00

males of 0.85 (7) 33 0.12 (7) 9 0.73 similar body 1.00 (38) 56 0.12 (65) 95 0.88 mass N = 4 0.97 (69) 64 0.19 (92) 62 0.78 0.40 (5) 42 0.00 (4) 34 0.40

fulfilled, no more fights occurred and males kept their status until the end of experiment. Since the dominance relationship was never reversed it could be considered as "stable" under these experimental conditions. A flow diagram of antagonistic behaviours between two males that occurred once the relation was established is shown in figure 1. This figure specifies behavioural sequences between a dominant and a subordinate male C. philander. Whereas the dominant male is indifferent to the approach of the other male, the latter exhibits a spontaneous escape behaviour, sometimes followed by distress calls when the dominant male cornes too close. Threatening pattern is typical in this species: a wide-open mouth and emission of loud vocalization oftenin a raised posture. Threats are few, but very efficient and lead the subordinate male to look for a shelter on the ground, in an empty nest-box or an empty cage.

342 Figure 1. - Flow diagram of the antagonistic male/male interactions occurring when a dominance­ submission relation was established. Frame size is proportional to the number of acts performed and arrow size is proportional to % of interaction. Dominant male �, Subordinate male � (% of the total number of interactions observed between males in ali groups, N = 16)

NUMBER OF FIGHTS AND TIME BEFORE DOMINANCE SETTLEMENT

In 16 groups a dominance-submission relationship was considered as established (difference in Id between the two competing males � 0.5). We compared four groups: males alone of similar and different body mass, and males of similar and different body mass with a female.

343 Time before seulement of the dominance relationship was different between groups (Kruskall-Wallis, x2 = 7.8, p = 0.05). The relationship was settled after a longer period of time in male/female groups compared to groups with males al one (multiple comparison, p < 0.05). This period varies from 1 to 4 weeks in male/female groups and is of 1 week in groups of males alone. The number of fights was not significantly different between groups 2 (Kruskall-Wallis, x = 3.8, p = 0.28), the total number of fights observed vary from 0 to 62 in the 16 different groups.

INFLUENCE OF MALE BODY MASS AND PLASMA CONCENTRATION OF TESTOSTER­ ONE ON SOCIAL RANK

As in other didelphid species, growth in body mass and body length is continuous (Atramentowicz, 1986), and older individuals are mainly heavier. In

this study, body mass and age were significantly correlated in males (n = 15,

rs = 0.59, Spearman test p = 0.02). Relation between dominance index (Id) and body mass and plasma concen­ tration of testosterone (measures recorded two days before the beginning of the first experiment) was tested with a Spearman rank correlation. In male groups with similar body mass, no significant correlation emerged

between dominance index (Id) and plasma concentration of testosterone (rs = 0.3,

n = 12). In male groups with different body mass, the dominance index was not significantly correlated with testosterone concentration in blood plasma, but

positively correlated with body mass (rs = 0.66; n = 24; p < 0.001) and age

(r8 = 0.5; n = 24; p < 0.05). Heavier and older males exhibited a higher dominance index.

INFLUENCE OF MALE SOCIAL RANK ON PHYSIOLOGICAL AND BEHAVIOURAL PA RAMETERS

The influence of social status on physiological and behavioural parameters was compared between dominant and subordinate males in four groups: males alone of similar and different body mass, and males of similar and differentbody mass with a female. As no significant difference was found (Kruskall-Wallis,

p = ns), the influence of social status was then investigated for ali individuals:

dominant males (n = 16) were compared to subordinate males (n = 16). To test the influence of social status on body mass, blood hematocrit and testosterone concentration (Fig. 2), we recorded variations between the first and the fourth week. Most males lost weight from the onset to the end of each experiment, without any significant difference between dominant and subordinate

males (- 12 ± 19 g and - 11 ± 31 g). Individual variations of hematocrit and testosterone concentration in blood were very important. Despite these important individual differences, the evolution of these physiological parameters was significantly different for subordinate and dominant males. The decrease in hematocrit, between the first and the fourth week of experiment, was higher in

subordinate males than in dominant ones (- 1.7 ± 4.2 % and -5.4 ± 3.9 %

respectively; U test, p = 0.02). During the first week, dominant males exhibited a sensible though not significant higher testosterone blood concentration than subordinate males (4.0 ± 2.7 ng/ml and 2.6 ± 1.3 ng/ml; U test o.s.). Testosterone

- 344 - level diminished significantly more in dorrtinant males during the experiment compared to subordinate males (- 1.8 ± 2.8 ng/ml and - 0.2 ± 1.1 ng/ml respec­

tive! y; U test, p = 0.05).

6

,-.._

�s:: 5 .._., r=-4 s:: 4,1 -� 4 � � � Q) () s:: 3 0 () .2,4 Q) i � s:: 2,6 2,3 8 2 l 1 Q) - "' 0 - "' Q) E-< 2 3 4 1 Weeks

Figure 2. - Variation in hematocrit and testosterone concentration in blood in dominant (D) and subordinate (s) males (N pairs of males = 16). Mean ± s.d. are given for the four weeks of experimental encounters.

345 Activity rate and scent-marking frequency were similar in dominant and subordinate males (A = 86 ± 40 and 68 ± 27, Fig. 3, and scent-marking/hours = 0.40 ± 0.48 and 0.35 ± 0.29 respectively). Nevertheless smelling-licking, which represents 73 % on average of the individual behaviours, was significantly more frequent in dominant males than in subordinate ones ( 48 ± 28 and 32 ± 20/hour; U test, p < 0.05; Fig. 3). The number of other behaviours (eating, drinking, excreting, grooming) was too low to perform separate calculations.

D dominant

• subordinate 100

1-< 80 * ;:::s 0 ...s:: 1-< (IJ o.. 60 (/) ...... � 4-< 0 40 1-< (IJ

� 20 z

total activity smelling-licking (except social interractions)

Figure 3. - Influence of social status on behavioural parameters (in number of acts per hour). Dominant males (N = 16), subordinate males (N = 16); U-test * = p < 0.05 .

Twelve females were placed in male groups: eight with males of different body mass and four with males of equivalent body mass. All females lost weight during the four-week experiment: mean body mass decreased significantly from 368 ± 44 g during the first week, to 348 ± 44 g during the last week (Wilcoxon test, p < 0.05). Only two females did not exhibit cytological œstrus during the experiment. Moreover, no difference in female activity was obvious when œstrus occurred. Male-female interaction occurrence was 11 ± 9 interactions per hour and most of these interactions were aggressive 73 ± 25 %. Males frequently initiated interactions with females and they rarely threatened or aggressed females even when they are attacked repeatedly. Most of the male-female interactions ended by female avoidance or threat. Interactions between the dominant male and the female were less aggressive, compared to those against the subordinate male (Wilcoxon

346 - test, p < 0.05). Unfortunately, probably due to captivity conditions, only two females exhibited typical sexual interactions: sexual chase and mounting attempt by the dominant male exclusively, and only during occurrence of œstrus.

DISCUSSION

lt is apparent in this study that dominance is based on age and body mass in Caluromys philander under experimental conditions. Dominant males exhibit a lower decrease in hematocrit rate and a higher decrease in testosterone concen­ tration in blood; they display most of the offensive antagonistic behaviours, scan more actively the experimental cages and are engaged in fewer aggressive interactions with females compared to subordinate males. Caution must be used in extrapoling from the behaviour of captive to wild animais, particularly when using data from observations of small groups of individuals, because sorne phenomena may occur only under unnatural constraints. Nevertheless, these informations are particularly useful for noctumal, arboreal, small bodied neotropical species like C. philander for which direct observation of interactions in the wild is virtually not possible. In captive Woolly Opossum, body mass and age are important parameters to establish hierarchy and heavier and older males were dominant in groups of different body mass. This observation fits well with many others performed on mammalian species (marsupials: Braithwaite, 1974; Bradley et al. , 1980; Gan­ slosser, 1989; Ryser, 1990; Mallick et al. , 1994; rodents: Militzer, 1995; elephants: Poole, 1989; Grey Seal: Anderson & Fedak, 1985 and Elephant Seal: Haley, 1994). The existence of a settled dominance between males of similar body size show that other indicators of dominance, as experience or aggressivity for example, should play a role in the probability of winning contests. In this species it is not possible to isolate confounding effects of age and body size since growth goes on · throughout adulthood (Atramentowicz, 1986). Nevertheless, data collected on a natural population of Didelphis virginiana in Florida, a relatively close species, show that "outcome of fightswas strongly inftuencedby body mass, but there was no influence of age" (Ryser 1992). In Caluromys philander, dominance­ submission relationships exist between males even without females. Nevertheless, inter-male competition is stronger when a female is present at close vicinity as in macropodid marsupials (Ganslosser, 1989). When dominance was settled, dominance rank was clear-cut and consistent during ali the experimentation. Stable dominance-subordination relationships may benefit both dominants and subordinates by minimizing the incidence of serious wounds (de Waal, 1982). Display, as territorial marking or threat, could also avoid potentially dangerous fighting. In Caluromys philander, as in Didelphis virginiana (Ryser, 1992), no limits to wounds occur, on the opposite to macropodid marsupials where animais test their strength in ritualized fights without risking severe injuries (Ganslosser, 1989). In our experiment, males showed typical signs of social stress as described by Von Holst (1977) in Tupaia belangeri (Scandentia, Tupaiidae): both body weight and hematocrit rate decrease. This could be due to a density effectassocia ted with a psychological effect tied-up with social status or Joss of aggressive interactions. Psychological effect could explain that hematocrit of subordinate males decreases

- 347 more than in dominant ones. In Didelphis virginiana (Holmes, 1987), subordinates are more stressed than dominants. During our experiment, the physical condition of males declined but none died, as it may happen in other marsupial species as D. virginiana (Ryser, 1990) and Antechinus stuartii (Braithwaite, 1974; Bradley et al., 1980). The decrease in testosterone concentration observed in ail males probably resulted from stress (Von Holst, 1977) and inter-male inhibition (Atramentowicz, unpublished data). Small differences occur in behaviour between dominant and subordinate males. No differences were found in global activity, or scent-marking, but dominant males scan more the experimental cages and exhibit more smelling­ licking behaviours than subordinates. In other marsupial species, D. virginiana or Petaurus breviceps, the social status had a marked influence on behaviour. In these species, dominant males scent-mark more, are more active and mobile (Holmes, 1987; Ryser 1990; Mallick et al. , 1994; Stoddart et al. , 1994). In the Woolly Opossum, males and females show principally indifferent and avoidance behaviours, and mating rarely occurs if they are in continuous contact. Therefore, intermittent contact was chosen in our experimental procedure ( 48 h each week). A stress due to a density effect could explain the lack of mating and pregnancy, as in mice (Bronson, 1989). Furthermore, females exhibited a reduced physical condition (weight loss) which is characteristic of stressed animais. Even if an influence of dominance upon mating success could not be demonstrated in our study, in the two groups where sexual interactions were performed, these happened only between a female and a dominant male. Interactions are less aggressive between females and dominant males than with subordinates. This difference in females aggressivity should be an important factor in determining access to mate in opossum species. In Caluromys philander, as in Didelphis virginiana (McManus 1970, Holmes 1987), females indicate copulatory readiness only by a lack of aggression toward males.

ACKNOWLEDGEMENTS

We are grateful to M. Perret, J.F. Ponge and M. Théry who greatly improved by constructive comments an earlier draft of this manuscript.

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349